Abstract

It is commonly assumed that dead pericarps of dry indehiscent fruits have evolved to provide an additional physical layer for embryo protection and as a means for long distance dispersal. The pericarps of dry fruits undergo programmed cell death (PCD) during maturation whereby most macromolecules such DNA, RNA, and proteins are thought to be degraded and their constituents remobilized to filial tissues such as embryo and endosperm. We wanted to test the hypothesis that the dead pericarp represents an elaborated layer that is capable of storing active proteins and other substances for increasing survival rate of germinating seeds. Using in gel assays we found that dead pericarps of both dehiscent and indehiscent dry fruits of various plant species including Arabidopsis thaliana and Sinapis alba release upon hydration multiple active hydrolytic enzymes that can persist in an active form for decades, including nucleases, proteases, and chitinases. Proteomic analysis of indehiscent pericarp of S. alba revealed multiple proteins released upon hydration, among them proteases and chitinases, as well as proteins involved in reactive oxygen species (ROS) detoxification and cell wall modification. Pericarps appear to function also as a nutritional element-rich storage for nitrate, potassium, phosphorus, sulfur, and others. Sinapis alba dehiscent and indehiscent pericarps possess germination inhibitory substances as well as substances that promote microbial growth. Collectively, our study explored previously unknown features of the dead pericarp acting also as a reservoir of biological active proteins, and other substances capable of “engineering” the microenvironment for the benefit of the embryo.

Highlights

  • Angiosperm evolution has led to the development of diverse fruit morphologies to assist seed dispersal [1]

  • In light of recent findings demonstrating that dead seed coat and floral bracts in grasses function as storage for hydrolytic enzymes [17,18], we investigated the capacity of dead pericarps of dry fruits for storing and releasing hydrolytic enzymes upon hydration

  • We examined S. alba dehiscent and indehiscent pericarps for nuclease activities by using in gel nuclease assay in the presence of Ca2+ and Mg2+ as cofactors in comparison with nucleases released from their corresponding seeds [18]

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Summary

Introduction

Angiosperm evolution has led to the development of diverse fruit morphologies to assist seed dispersal [1]. Dry fruits consist of two major groups, dehiscent in which the fruit splits open at maturity to allow for seed dispersal, and indehiscent whereby the fruit is not opened at maturity and constitutes the dispersal unit. The pericarp is developed from the ovary wall or ovary wall, plus some accessory parts and this region comprises of an outer layer, the exocarp, the middle layer, the mesocarp, and the inner layer, the endocarp, which is distinct in fleshy fruits; in dry fruits, the subdivisions of the pericarp are not clear [3]. Maternal tissues enclosing the embryo such as the nucellus, the seed coat, the pericarp, and the nucellar projections undergo a progressive degeneration by programmed cell death (PCD). As a result macromolecules such as DNA, RNA and proteins are degraded and their constituents remobilized to filial tissues like endosperm and the embryo [4]

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